Ancient viral genomes reveal introduction of human pathogenic viruses into Mexico during the transatlantic slave trade

  1. Axel A Guzmán-Solís
  2. Viridiana Villa-Islas
  3. Miriam J Bravo-López
  4. Marcela Sandoval-Velasco
  5. Julie K Wesp
  6. Jorge A Gómez-Valdés
  7. María de la Luz Moreno-Cabrera
  8. Alejandro Meraz
  9. Gabriela Solís-Pichardo
  10. Peter Schaaf
  11. Benjamin R tenOever
  12. Daniel Blanco-Melo  Is a corresponding author
  13. María C Ávila Arcos  Is a corresponding author
  1. Universidad Nacional Autónoma de México, Mexico
  2. University of Copenhagen, The Globe Institute, Denmark
  3. North Carolina State University, United States
  4. Instituto Nacional de Antropología e Historia, Mexico
  5. Icahn School of Medicine at Mount Sinai, United States
  6. Fred Hutchinson Cancer Research Center, United States

Abstract

After the European colonization of the Americas there was a dramatic population collapse of the Indigenous inhabitants caused in part by the introduction of new pathogens. Although there is much speculation on the etiology of the Colonial epidemics, direct evidence for the presence of specific viruses during the Colonial era is lacking. To uncover the diversity of viral pathogens during this period, we designed an enrichment assay targeting ancient DNA (aDNA) from viruses of clinical importance and applied it to DNA extracts from individuals found in a Colonial hospital and a Colonial chapel (16th c. - 18th c.) where records suggest victims of epidemics were buried during important outbreaks in Mexico City. This allowed us to reconstruct three ancient human parvovirus B19 genomes, and one ancient human hepatitis B virus genome from distinct individuals. The viral genomes are similar to African strains, consistent with the inferred morphological and genetic African ancestry of the hosts as well as with the isotopic analysis of the human remains, suggesting an origin on the African continent. This study provides direct molecular evidence of ancient viruses being transported to the Americas during the transatlantic slave trade and their subsequent introduction to New Spain. Altogether, our observations enrich the discussion about the etiology of infectious diseases during the Colonial period in Mexico.

Data availability

Reconstructed genomes from this study are available in Genbank under accession number MT108214, MT108215, MT108216, MT108217. NGS reads used to reconstruct ancient viral genomes reported in this study are available in Dryad (https://doi.org/10.5061/dryad.5x69p8d2s).

The following data sets were generated

Article and author information

Author details

  1. Axel A Guzmán-Solís

    International Laboratory for Human Genome Research, Universidad Nacional Autónoma de México, Querétaro, Mexico
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6878-206X
  2. Viridiana Villa-Islas

    International Laboratory for Human Genome Research, Universidad Nacional Autónoma de México, Querétaro, Mexico
    Competing interests
    The authors declare that no competing interests exist.
  3. Miriam J Bravo-López

    International Laboratory for Human Genome Research, Universidad Nacional Autónoma de México, Querétaro, Mexico
    Competing interests
    The authors declare that no competing interests exist.
  4. Marcela Sandoval-Velasco

    Section for Evolutionary Genomics, University of Copenhagen, The Globe Institute, Copenhagen, Denmark
    Competing interests
    The authors declare that no competing interests exist.
  5. Julie K Wesp

    Department of Sociology and Anthropology, North Carolina State University, Raleigh, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Jorge A Gómez-Valdés

    ENAH, Instituto Nacional de Antropología e Historia, Mexico City, Mexico
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6996-2732
  7. María de la Luz Moreno-Cabrera

    NA, Instituto Nacional de Antropología e Historia, Mexico City, Mexico
    Competing interests
    The authors declare that no competing interests exist.
  8. Alejandro Meraz

    NA, Instituto Nacional de Antropología e Historia, Mexico City, Mexico
    Competing interests
    The authors declare that no competing interests exist.
  9. Gabriela Solís-Pichardo

    Laboratorio Universitario de Geoquímica Isotópica (LUGIS), Instituto de Geología, Universidad Nacional Autónoma de México, Mexico City, Mexico
    Competing interests
    The authors declare that no competing interests exist.
  10. Peter Schaaf

    LUGIS, Instituto de Geofísica, Universidad Nacional Autónoma de México, Mexico City, Mexico
    Competing interests
    The authors declare that no competing interests exist.
  11. Benjamin R tenOever

    Microbiology, Icahn School of Medicine at Mount Sinai, New York, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0324-3078
  12. Daniel Blanco-Melo

    Microbiology, Fred Hutchinson Cancer Research Center, Seattle, United States
    For correspondence
    dblancom@fredhutch.org
    Competing interests
    The authors declare that no competing interests exist.
  13. María C Ávila Arcos

    International Laboratory for Human Genome Research, Universidad Nacional Autónoma de México, Querétaro, Mexico
    For correspondence
    mavila@liigh.unam.mx
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1691-1696

Funding

Welcome Trust Sanger (208934/Z/17/Z)

  • María C Ávila Arcos

PAPIIT-DGAPA-UNAM (IA201219)

  • María C Ávila Arcos

Human Frontier Science (RGY0075/2019)

  • María C Ávila Arcos

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. George H Perry, Pennsylvania State University, United States

Ethics

Human subjects: Permission to process these samples were provided by the INAH Archeology Council with numbers 401.1S.3-2018/1373 and 401.1S.3-2020/1310 for the Hospital San Jose de los Naturales and the Temple of Immaculate Conception (La Conchita), respectively.

Version history

  1. Preprint posted: June 6, 2020 (view preprint)
  2. Received: March 21, 2021
  3. Accepted: July 30, 2021
  4. Accepted Manuscript published: August 5, 2021 (version 1)
  5. Version of Record published: September 7, 2021 (version 2)

Copyright

© 2021, Guzmán-Solís et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Axel A Guzmán-Solís
  2. Viridiana Villa-Islas
  3. Miriam J Bravo-López
  4. Marcela Sandoval-Velasco
  5. Julie K Wesp
  6. Jorge A Gómez-Valdés
  7. María de la Luz Moreno-Cabrera
  8. Alejandro Meraz
  9. Gabriela Solís-Pichardo
  10. Peter Schaaf
  11. Benjamin R tenOever
  12. Daniel Blanco-Melo
  13. María C Ávila Arcos
(2021)
Ancient viral genomes reveal introduction of human pathogenic viruses into Mexico during the transatlantic slave trade
eLife 10:e68612.
https://doi.org/10.7554/eLife.68612

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https://doi.org/10.7554/eLife.68612

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